The Science of Nature

, 104:1 | Cite as

Bone histology sheds light on the nature of the “dermal armor” of the enigmatic sauropod dinosaur Agustinia ligabuei Bonaparte, 1999

  • Flavio BellardiniEmail author
  • Ignacio A. Cerda
Original Paper


Agustinia ligabuei is an Early Cretaceous sauropod dinosaur from the northwest of Patagonia that is currently the topic of debate with respect to its phylogenetic position and atypical dermal armor. The presence of four morphotypes of laminar and transversely elongated putative osteoderms was used to consider Agustinia as an armored sauropod. Regarding the different hypotheses about the identity of the bony structures of Agustinia (e.g., osteoderms, cervical or dorsal ribs, hypertrophied elements), a comparative histological analysis has been carried out. Histological evidence is presented herein and reveals that none of the morphotypes of Agustinia shows a primary bone tissue formed by structural fiber bundles as in other sauropod dinosaur osteoderms. Furthermore, on the basis of their gross morphology and microstructure, the bony structures originally classified as types 1 + 4 and 3 are more comparable respectively with dorsal and cervical ribs than any other kind of dermal or bony element. Due to poor preservation, the nature of the type 2 cannot be assessed but is here tentatively assigned to a pelvic girdle element. Although a phylogenetic reassessment of Agustinia is not the purpose of this paper, our paleohistological analyses have broader implications: by not supporting the dermal armor hypothesis for Agustinia, its inclusion in Lithostrotia is not justified in the absence of other diagnostic features.


Early cretaceous Sauropoda Osteoderms Bone microstructure Mineralized fibers Metaplasia 



Museo Municipal “Carmen Funes” de Plaza HuinculPalaeovertebrate collection Plaza Huincul, Neuquén Province, Argentina


Museo de Cinco Saltos, Palaeohistological collection, Cinco Saltos, Rio Negro Province, Argentina


Museo de Cinco Saltos, Palaeovertebrate collection, Cinco Saltos, Rio Negro Province, Argentina


Museo Provincial ‘Carlos Ameghino’, Palaeohistological collection, Cipolletti, Rio Negro Province, Argentina


Museo Provincial ‘Carlos Ameghino,’ Palaeovertebrate collection, Cipolletti, Río Negro Province, Argentina


Paleovertebrate collection of Instituto Miguel Lillo, Tucumán Province, San Miguel de Tucumán, Argentina


Paleohistology collection of Instituto Miguel Lillo, Tucumán Province, San Miguel de Tucumán, Argentina



We thank J. Bonaparte and A. Martinelli for providing helpful information, comments, original field-work photos, and field notes, as well in helping us to reconstruct the taphonomy of holotype materials of Agustinia; the Dirección Provincial de Patrimonio Cultural of Neuquén and the Museo Municipal Carmen Funes of Plaza Huincul for their collaboration, as well as legal and logistic support; J. Curruinca, S. Adrian, Sr. Firelli, and the Municipalidad of Picún Leufú for allowing the access at the Cerro Leon locality and to support part of the field works; R.A. Coria of MCF for the collection access and E. Montes for preparing part of the material; D. Codega of USL for making the thin sections; J. Carballido, P. Mannion, M. D’Emic, and an anonymous reviewer for providing constructive criticism and suggestions that improved the original manuscript. J. Blanco kindly provided the Agustinia reconstruction for Fig. 1. A. Elbakyan, J. Bar, and Wikipaleo Group provided the literature. This project has been partially funded by Jurassic Foundation (Grant to F. B) and Agencia Nacional de Promoción Científica y Técnica (PICT 2015-1021 to I.A.C).


  1. Apesteguía S (2004) Bonitasaura salgadoi gen. et sp. nov.: a beaked sauropod from the late cretaceous of Patagonia. Naturwissenschaften 91:493–497. doi: 10.1007/s00114-004-0560-6 CrossRefPubMedGoogle Scholar
  2. Barrett PM, Clarke JB, Brinkman DB, Chapman SD, Ensom PC (2002) Morphology, histology and identification of the ‘granicones’ from the Purbeck Limestone Formation (Lower Cretaceous: Berriasian) of Dorset, southern England. Cretac Res 23(2):279–295. doi: 10.1006/cres.2002.1002
  3. Bonaparte JF (1999) An armoured sauropod from the Aptian of northern Patagonia, Argentina. National Science Museum Monographs 15:1–12Google Scholar
  4. Bonaparte JF, Powell J (1980) A continental assemblage of tetrapods from the upper cretaceous of northwestern Argentina (Sauropoda-Coelurosauria-Carnosauria-Aves). Mémories de la Société Géologique de France 139:19–28Google Scholar
  5. Borsuk-Bialynicka M (1977) A new camarasaurid sauropod Opisthocoelicaudia skarzynskii gen. n., sp. n. from the upper cretaceous of Mongolia. Palaeontol Pol 37:5–64Google Scholar
  6. Britt BB (1997) Postcranial pneumaticity. In: Currie PD, Padian K (eds) The encyclopedia of dinosaurs. New York Academic Press, New York, pp. 590–593Google Scholar
  7. Burns ME, Currie PJ (2014) External and internal structure of ankylosaur (Dinosauria; Ornithischia) osteoderms and their systematic relevance. J Vertebr Paleontol 34:835–851. doi: 10.1080/02724634.2014.840309 CrossRefGoogle Scholar
  8. Burns ME, Vavrek MJ (2014) Probable ankylosaur ossicles from the middle Cenomanian Dunvegan formation of northwestern Alberta, Canada. PLoSONE 9(5):e96075. doi: 10.1371/journal.pone.0096075 CrossRefGoogle Scholar
  9. Carrano MT, D’Emic MD (2015) Osteoderms of the titanosaur sauropod dinosaur Alamosaurus sanjuanensis Gilmore, 1922. J Vertebr Paleontol. doi: 10.1080/02724634.2014.901334 Google Scholar
  10. Carrano MT, Hutchinson JR (2002) Pelvic and hind limb musculature of Tyrannosaurus rex (Dinosauria: Theropoda). J Morphol 253:207–228. doi: 10.1002/jmor.10018 CrossRefPubMedGoogle Scholar
  11. Cerda IA (2009) Consideraciones sobre la histogénesis de las costillas cervicales en los dinosaurios saurópodos. Ameghiniana 46:193–198Google Scholar
  12. Cerda IA, Powell JE (2010) Dermal armor histology of Saltasaurus loricatus, an upper cretaceous sauropod dinosaur from Northwest Argentina. Acta Paleontologica Polonica 55:389–398. doi: 10.4202/app.2009.1101 CrossRefGoogle Scholar
  13. Cerda IA, Casal GA, Martinez RD, Ibiricu LM (2015a) Histological evidence for a supraspinous ligament in sauropod dinosaurs. Royal Society Open Science 2:150369. doi: 10.1098/rsos.150369 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Cerda IA, García RA, Powell JE, Lopez O (2015b) Morphology, microanatomy, and histology of titanosaur (Dinosauria, Sauropoda) osteoderms from the upper cretaceous of Patagonia. J Vertebr Paleontol 35(1):e905791. doi: 10.1080/02724634.2014.905791 CrossRefGoogle Scholar
  15. Chinsamy A, Raath MA (1992) Preparation of fossil bone for histological examination. Palaeontol Afr 29: 39–44.Google Scholar
  16. Chinsamy-Turan A (2005) The microstructure of dinosaur bone: deciphering biology with fine-scale techniques. Johns Hopkins University Press, Baltimore, p. 195. doi: 10.1111/j.1096-3642.2008.00476.x Google Scholar
  17. Curry Rogers K (2005) Titanosauria, a phylogenetic overview. In: Curry Rogers K, Wilson JA (eds) The sauropods: evolution and Paleobiology. University of California Press, Berkley, pp. 50–103Google Scholar
  18. D’Emic MD, Wilson JA, Chatterjee S (2009) The titanosaur (Dinosauria: Sauropoda) osteoderm record: review and first definitive specimen from India. J Vertebr Paleontol 29(1):165–177. doi: 10.1671/039.029.0131 CrossRefGoogle Scholar
  19. Francillon-Vieillot H, Bufrenil V, Castanet J, Geraudie J, Meunier FJ, Sire JY, Zylberberg L, de Ricqlès A (1990) Microstructures and mineralization of vertebrate skeletal tissues. In: Carter J (ed) Skeletal biomineralization: patterns, process and evolutionary trends. Van Nostrand Reinhold, New York, pp. 471–530. doi: 10.1029/SC005p0175 Google Scholar
  20. Gallina PA (2012) Histología ósea del titanosaurio Bonitasaura salgadoi (Dinosauria: Sauropoda) del Cretácico Superior de Patagonia. Ameghiniana 49:289–302. doi: 10.5710/amgh.v49i3(519) CrossRefGoogle Scholar
  21. Hill RV (2006) Comparative anatomy and histology of xenarthran osteoderms. J Morphol 267(12):1441–1460. doi: 10.1002/jmor.10490 CrossRefPubMedGoogle Scholar
  22. Horner JR, Woodward HN, Bailleul AB (2016) Mineralized tissues in dinosaurs interpreted as having formed through metaplasia: a preliminary evaluation. Comptes Rendus Palevol 15(1–2):176–196. doi: 10.1016/j.crpv.2015.01.006 CrossRefGoogle Scholar
  23. Klein N, Christian A, Sander PM (2012) Histology shows that elongated neck ribs in sauropod dinosaurs are ossified tendons. Biol Lett. doi: 10.1098/rsbl.2012.0778 PubMedPubMedCentralGoogle Scholar
  24. Lacovara KJ, Ibiricu LM, Lamanna MC, Poole JC, Schroeter ER, Ullmann PV, Voegele KK, Boles ZM, Egerton VM, Harris JD, Martínez RD, Novas FE (2014) A gigantic, exceptionally complete titanosaurian sauropod dinosaur from southern Patagonia, Argentina. Scientific Reports 4(6196):1–9. doi: 10.1038/srep06196 Google Scholar
  25. Leanza HA, Apesteguía S, Novas FE, de la Fuente MS (2004) Cretaceous terrestrial beds from the Neuquén basin (Argentina) and their tetrapod assemblages. Cretac Res 25:1–96. doi: 10.1016/j.cretres.2003.10.005 CrossRefGoogle Scholar
  26. Mannion PD, Upchurch P, Barnes RN, Mateus O (2013) Osteology of the late Jurassic Portuguese sauropod dinosaur Lusotitan atalaiensis (Macronaria) and the evolutionary history of basal titanosauriforms. Zool J Linnean Soc 168(1):98–206. doi: 10.1111/zoj.12029 CrossRefGoogle Scholar
  27. Martinelli AG, Garrido AC, Forasiepi AM, Paz ER, Gurovich Y (2007) Notes on fossil remains from the early cretaceous Lohan Cura formation, Neuquén Province, Argentina. Gondwana Res 11(4):537–552. doi: 10.1016/ CrossRefGoogle Scholar
  28. Martínez RD, Giménez O, Rodriguez J, Luna M, Lamanna MC (2004) An articulated specimen of the basal titanosaurian (Dinosauria: Sauropoda) Epachthosaurus sciuttoi from the early late cretaceous Bajo Barreal formation of Chubut Province, Argentina. J Vertebr Paleontol 24:107–120. doi: 10.1671/9.1 CrossRefGoogle Scholar
  29. Molnar RE (2011) New morphological information about cretaceous sauropod dinosaurs from the Eromanga Basin, Queensland, Australia. Alcheringa 35:329–339. doi: 10.1080/03115518.2011.533978 CrossRefGoogle Scholar
  30. Novas FE (2009) The age of dinosaurs in South America. Indiana University Press, Bloomington, p. 437 ISBN 978-0-253-35289-7Google Scholar
  31. Organ CL, Adams J (2005) The histology of ossified tendons in dinosaurs. J Vertebr Paleontol 25:602–613. doi: 10.1671/0272-4634(2005)025 CrossRefGoogle Scholar
  32. Remes K, Ortega F, Fierro I, Joger U, Kosma R et al (2009) A new basal sauropod dinosaur from the middle Jurassic of Niger and the early evolution of Sauropoda. PLoS One 4(9):e6924. doi: 10.1371/journal.pone.0006924 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Saegusa H, Ikeda T (2014) A new titanosauriform sauropod (Dinosauria: Saurischia) from the Lower Cretaceous of Hyogo, Japan. Zootaxa 3848(1):1–66. doi: 10.11646/zootaxa.3848.1.1 
  34. Salgado L (2003) Considerations on the bony plates assigned to titanosaurs (Dinosauria, Sauropoda). Ameghiniana 40:441–456Google Scholar
  35. Salgado L, Bonaparte JF (2007) Sauropodomorpha. In: Gasparini ZS, Salgado L, Coria RA (eds) Patagonian mesozoic reptiles. Indiana University Press, pp 188–228.Google Scholar
  36. Sanz JL, Powell JE, Le Loeuff J, Martínez R, Pereda Suberbiola X (1999) Sauropod remains from the upper cretaceous of Laño (northcentral Spain). Titanosaur phylogenetic relationships. Estudios del Museo de Ciencias Naturales de Alava 14(1):235–255Google Scholar
  37. Scheyer TM, Sander PM (2004) Histology of ankylosaur osteoderms: implications for systematics and function. J Vertebr Paleontol 20:874–893. doi: 10.1671/0272-4634(2004)024 CrossRefGoogle Scholar
  38. Taylor MP (2009) Aspects of the history, anatomy, taxonomy and palaeobiology of sauropod dinosaurs. PhD thesis, University of Portsmouth, Portsmouth, England, pp 285.Google Scholar
  39. Upchurch P, Barrett PM, Dodson P (2004) Sauropoda. In: Weishampel DB, Dodson P, Osmólska H (eds) The Dinosauria, 2nd edn. University of California Press, Berkeley, pp. 259–324CrossRefGoogle Scholar
  40. Vickaryous MK, Hall BK (2006) Osteoderm morphology and development in the nine-banded armadillo, Dasypus novemcinctus (Mammalia, Xenarthra, Cingulata). J Morphol 267(11):1273–1283. doi: 10.1002/jmor.10475 CrossRefPubMedGoogle Scholar
  41. Vickaryous MK, Hall BK (2008) Development of the dermal skeleton in Alligator mississippiensis (Archosauria, Crocodylia) with comments on the homology of osteoderms. J Morphol 269(4):398–422. doi: 10.1002/jmor.10575 CrossRefPubMedGoogle Scholar
  42. Vickaryous MK, Sire JY (2009) The integumentary skeleton of tetrapods: origin, evolution, and development. J Anat 214:441–464. doi: 10.1111/j.1469-7580.2008.01043.x CrossRefPubMedPubMedCentralGoogle Scholar
  43. Vickaryous MK, Meldrum G, Russell AP (2016) Armored geckos: a histological investigation of osteoderm development in Tarentola (Phyllodactylidae) and Gekko (Gekkonidae) with comments on their regeneration and inferred function. J Morphol 276:1345–1357. doi: 10.1002/jmor.20422 CrossRefGoogle Scholar
  44. Waskow K, Sander PM (2014) Growth record and histological variation in the dorsal ribs of Camarasaurus sp. (Sauropoda). J Vertebr Paleontol 34(4):852–869. doi: 10.1080/02724634.2014.840645 CrossRefGoogle Scholar
  45. Wedel MJ (2003) Vertebral pneumaticity, air sacs, and the physiology of sauropod dinosaurs. Paleobiology 29:243–255. doi: 10.1017/S0094837300018108 CrossRefGoogle Scholar
  46. Wilson JA (2002) Sauropod dinosaur phylogeny: critique and cladistic analysis. Zool J Linnean Soc 136:217–276. doi: 10.1046/j.1096-3642.2002.00029.x CrossRefGoogle Scholar
  47. Witzmann F, Soler-Gijón R (2010) The bone histology of osteoderms in temnospondyl amphibians and in the chroniosuchian Bystrowiella. Acta Zool 91(1):96–114. doi: 10.1111/j.1463-6395.2008.00385.x CrossRefGoogle Scholar
  48. Zhang Y (1988) The middle Jurassic dinosaur fauna from Dashanpu, Zigong, Sichuan: sauropod dinosaurs. Vol. 1, Shunosaurus. Sichuan Publishing House of Science and Technology, Chengdu, p. 89Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Museo Municipal “Carmen Funes”Plaza HuinculArgentina
  2. 2.Dirección Provincial de Patrimonio CulturalNeuquénArgentina
  3. 3.CONICET, Instituto de Investigaciones en Paleobiología y GeologíaUniversidad Nacional de Río NegroCipollettiArgentina

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